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Abstract

Background

Few studies have evaluated the linkage between food cost and mortality among older
adults. This study considers the hypothesis that greater food expenditure in general,
and particularly on more nutritious plant and animal-derived foods, decreases mortality
in older adults.

Methods

This study uses the 1999–2000 Elderly Nutrition and Health Survey in Taiwan and follows
the cohort until 2008, collecting 24-hr dietary recall data for 1781 participants
(874 men and 907 women) aged 65 y or older. Using monthly mean national food prices
and 24-hr recall, this study presents an estimate of daily expenditures for vegetable,
fruit, animal-derived, and grain food categories. Participants were linked to the
national death registry.

Results

Of the 1781 original participants, 625 died during the 10-y follow-up period. Among
the 4 food categories, the fourth and fifth expenditure quintiles for vegetables and
for fruits had the highest survival rates. After adjusting for co-variates, higher
(Q4) vegetable and higher fruit (Q4) food expenditures referent to Q1 were significantly
predictive of reduced mortality (HR = 0.55, 95% CI: 0.39-0.78 and HR = 0.64, 95% CI:
0.42–0.99, respectively) and the risk decreased by 12% and 10% for every NT$15 (US$0.50)
increase in their daily expenditures. Animal-derived and grain food spending was not
predictive of mortality.

Conclusion

Greater and more achievable vegetable and fruit affordability may improve food security
and longevity for older adults.

Keywords:

Food expenditure; Mortality; Elders; Vegetables

Introduction

The gains in public health achieved over the past few decades are currently threatened
by the global economic and food crises, with young children, women, and older adults
in the developing world likely to be disproportionately affected [1]. Poorer households facing food insecurity may be in fear or running out of food or
money to buy food and face food scarcity because of economic decline. In many cases,
they purchase cheaper foods than usual or simply go without food for a day or more
for economic reasons [2]. Some older people are at risk of malnutrition because of food insufficiency, and
have lower mean intakes of various nutrients and lower intakes of vegetables and meat
and lower dietary variety [3]. Wealthy households have higher expenditures on animal-source foods, vegetables,
and fats and oils compared to moderately and severely food-insecure households [4]. Solutions to these dilemmas require further studies that merge health economics
and nutrition in the field of what might be called “nutritional economics” [5].

Most dietary studies have shown that greater vegetable, legumes, and fruit intakes
are linked to reduced risk of all-cause mortality in older populations [6-10]. Studies from Bangladesh show that when people spend more money on rice, child and
maternal malnutrition increases [11]. This may be because of a corresponding reduction in the intake of other plant foods,
such as fruit and vegetables and animal-derived food [11,12]. However, no study has investigated the relationship between expenditures on various
food groups and older adult all-cause mortality in a relatively affluent society such
as Taiwan. We hypothesize that the purchase of more expensive, albeit nutritious foods,
such as vegetables, fruits, and animal-derived foods might predict a lower risk of
mortality. Conversely, the purchase of less expensive commodities such as rice might
be linked to higher mortality in older adults. We tested this proposition by assessing
the food expenditure profiles of a cohort of older Taiwanese adults followed for 10
y and linked to the National Death Registry.

Methods

Study participants

The participants in this study were free-living, older adults aged 65 y or older and
involved in the nationally representative Elderly Nutrition and Health Survey in Taiwan
(NAHSIT) conducted between 1999 and 2000 [13,14]. A total of 1911 (955 men and 956 women) participants completed a 24-hr dietary recall
by interview at home. Participants were excluded if they reported extremely high or
low total daily energy intakes (<500 or >3500 kcal/d in women, <800 or > 4200 kcal/d
in men, n = 126), or if their diets comprised only liquid (mainly milk, n = 2). The
remaining participants were linked to the National Death Registry up to December 31,
2008. Two participants were excluded because of incorrect death records, leaving 1781
participants eligible for the final analysis [6,15].

Daily food expenditure

This study uses 24-hr dietary recall data collected on the survey day to calculate
participants’ intakes of specific foods [13]. The data included 3646 foods. For food price assignment, we combined, categorized,
and encoded similar food items as 843 foods. Food items were categorized according
to the same or similar names, similar nutrient profile, comparable food physical properties,
and similar ingredients irrespective of preparation. Each food was priced at the cost
per 100 g, as purchased. The cost of each food was determined from the Taiwanese Council
of Agriculture, databases from the Agriculture and Food Agency, Poultry and Livestock
Products Current Trade, and the Fisheries Agency from January 1999 to December 2000
expressed in retail prices (New Taiwan Dollars, NTD) [16-18]. All foods were matched with the national average monthly retail price (NTD/100 g)
based on participants’ interview dates. For foods not included in these sources, prices
were obtained from a widely available national supermarket chain with consistent prices
across Taiwan. In this case, regular 2009 prices listed were used without discount.
The supermarket prices of these goods were then deflated according to the Consumer
Price Index for 1999–2000. For the remaining foods without a known cost, proxy prices
were used based on the lowest food prices for the same food classification, or the
lowest food prices for products with similar ingredients. In total 215 of the 843
foods used this approach. Food costs did not include alcohol, drinking water, or condiments.
The food expenditure of participants was generated from these food costs with the
assumption that they ate at home. Previous research has presented a detailed description
of food price calculation [19]. Food expenditures were assigned to items in 1 of 4 categories: vegetables, consisting
of vegetables, beans, soybeans, and soybean products; fruits, consisting of fruit
and fresh fruit juices; animal-derived foods, consisting of chicken, duck, pork, beef,
goat, fish, and shellfish, eggs, and dairy; and grain foods, consisting of rice and
rice products, wheat and flour products, starchy roots and stems, dry beans, and dry
bean products. The daily food expenditure for each participant was derived for each
of these 4 categories (Table 1).

Statistical analysis

The 4 categories of daily food expenditures were classified into quintiles of energy-adjusted
dietary spending (NTD) using the residual method for energy adjustment [20]. Categorical variables were compared using chi-square tests. Cox proportional-hazards
models were used to examine the relationship between food expenditures and mortality.
The hazard ratios (HRs) and 95% confidence intervals (CIs) across quintiles for each
food category expenditure were compared to those of the lowest quintile. The 3 food
category expenditures for vegetables, fruits and grains and total food expenditure
were modeled simultaneously with the assumption that total food spending was fixed,
and with animal-derived foods excluded given their significantly higher cost. This
allowed the interpretability of the estimates of the other 3 categories of food in
the model. In other words, with fixed total food expenditure, one category must be
substituted for another. In this case, changes in animal-derived foods expenditure
would take preeminence, and the exclusion of the category enables evaluating the interplay
between vegetables, fruits, and grains, and their effects on mortality. In addition,
this study considers food category expenditures as continuous variables to assess
the survival consequences of each NT$15 per day, equivalent to US$0.50, increment
in various categories, considering other food category expenditures and total food
expenditure.

All analyses were conducted using SAS statistical software (version 8.0, 1999, SAS
Institute Inc, Cary, NC). SUDAAN (version 9.0, 2004, Triangle Park, NC) was used to
account for the sampling design. A value of p < 0.05 was considered significant.

Ethics

The protocol of this study: was approved by the ethics committees of both the Academia
Sinica and the National Health Research Institutes in Taiwan. All participants
provided signed informed consent.

Results

A total of 625 (35.9%) participants died during the 10-y follow-up. Table 1 shows the survival status in relation to each of the 4 food category expenditures.
The deceased in the highest 2 quintiles of vegetable expenditures were proportionately
lower (p = 0.009). However, almost 50% of the older adults in the first quintile were deceased.
The top 2 quintiles for fruit expenditures have significantly greater survivorship
than the lower expenditure quintiles (p < 0.001). The differences for animal-derived foods, for grains, and for total food
expenditure are not significant.

The cumulative death rates were 68.1 and 39.9 per 1000 person-years in the first and
the fifth quintiles of vegetable expenditures, respectively. The lowest rate was 36.3
in the fourth quintile (Table 2). Participants aged 80 y or older, indigenous, or who lived alone were more likely
to have lower expenditures on vegetables, and gender, education, and income produced
no significant differences. Participants whose chewing ability was satisfactory were
more likely to have higher vegetable expenditures; however, perceived health status
and physical activity were not significantly associated. The findings for fruits were
similar to those for vegetables (data not shown).

In the crude model, the HRs for all-cause mortality of the participants significantly
decreased as the expenditures of vegetables and fruits increased; however, no such
relationship for grains and animal-derived foods was observed. This pattern remains
after simultaneous adjustment for total food, vegetables, fruits, and grains expenditures,
age, and gender (Table 3). With further adjustments for potential co-variates, the Q4 and Q5 for vegetable
expenditure had HR values significantly lower than Q1 for all-cause mortality (Q4,
HR = 0.55, 95% CI: 0.39-0.78; Q5, HR = 0.74, 95% CI: 0.50-1.08), and the dose–response
relationship was significant. For fruits, Q3 and Q4 expenditures were associated with
significantly lower mortality rates compared to Q1 (Q3, HR = 0.62, 95% CI: 0.42-0.92;
Q4, HR = 0.64, 95% CI: 0.42-0.99), and the dose–response relationship remained significant
in the model 1. With further adjustment for DDS, the Q4 for vegetable expenditure
remained significant whereas it did not for fruit. For grains and animal-derived foods,
neither the HRs nor the linear trends were significant in the adjusted models.

When treating food expenditure as a continuous variable, every NT$15 increase in daily
vegetable or fruit expenditure led to 12% or 10% reductions, respectively, in all-cause
mortality, when holding total food and grains expenditures and potential co-variates
constant (Table 3). After excluding participants who died in the first year of follow-up, every NT$15
increase in daily vegetable expenditure caused a 16% reduction in all-cause mortality
(HR = 0.84, 95% CI: 0.72, 0.99). For fruit, every NT$15 increase in daily fruit expenditure
was associated with a 12% reduction in all-cause mortality (HR = 0.88, 95% CI: 0.77,
1.00).

Discussion

This study shows that vegetable and fruit expenditures are associated with less risk
of death in the elderly in Taiwan. Both of these expenditures are higher than that
for grains, but less than that for animal-derived foods. Contrary to the original
hypothesis, there was no identifiable association between animal or grain food costs
and all-cause mortality.

Vegetables and fruits are important sources of many bioactive components, including
polyphenols, carotenoids, folate, and vitamin C [21]. Whether these phytochemicals or micronutrients can explain the association between
vegetable and fruit expenditures and all-cause mortality in older adults remains unclear.
Research by the International Union of Nutritional Sciences Food Habits in Later life
(IUNS-FHILL) study shows that integrated indices of the diet, akin to a Mediterranean
diet score, can account for more of the link between diet and mortality than any other
food item, except for legumes, or specific nutrients [9 ,10]. Lee et al. found support
for this finding for food indices and mortality in Taiwan [6]. A study by the European Prospective Investigation into Cancer and Nutrition (EPIC)
showed a small inverse association between the intake of total fruits and vegetables
and cancer risk [22]
; a higher intake of fruits and vegetables is associated with a reduced risk of
ischemic heart disease mortality in the same cohort [23].

Evidence from rural Indonesia shows that households that spend a greater proportion
on plant foods have lower under-5 child mortality [24]. However, no study has focused on food expenditures in relation to older adult mortality.
Our study shows that vegetable and fruit expenditures had a protective effect on all-cause
mortality in elders. After controlling for potential confounders, the Q4 of vegetables
had a 45% lower all-cause mortality compared to those of the lowest quintile, and
for fruit had a 36% lower all cause mortality. With adjustment for dietary quality
(DDS), the significance of the HR for vegetables was unchanged, and that for fruits
diminished. This indicates a greater dependence on dietary diversity or an integrated
food pattern for fruit than for vegetable expenditure where the latter appears to
have associations with mortality of its own. In some respects, a vegetable mortality
link in Taiwan could have been relatively obscure. This is because the general population
eats vegetables, and especially green leafy vegetables and soybeans (as myriad forms
of tofu) extensively and regularly [6]. Thus, this might not have been a discriminating factor for survival difference.
However, seasonality and natural disasters, especially typhoons, can alter vegetable
supply dramatically and drive up prices quickly. This in turn makes vegetables unaffordable
for the economically marginalized, including some older adults. In the event, vegetable
costs in Taiwan are a survival discriminator for older adults. The finding of survival
advantage with greater vegetable expenditure makes the prospects of food security
for those with limited means and marginal vegetable supplies more achievable.

A possible reason the top quintile of vegetables has a higher HR than the fourth quintile
may be the diminishing marginal health benefit of vegetable intakes with their greater
consumption, “crowding out” other food commodities. Thus, the Q4 for vegetables may
represent optimal food expenditure among Taiwanese older adults for the greatest health
benefit (as judged by mortality). The mean for this Q4 for vegetables is 463 g/d for
fruit is 377 g/d, which meets the World Health Organization’s recommendations for
vegetable and fruit consumption [22]. However, once sufficiency is reached, those who consume more vegetables or fruit
(or even other food commodities) might improve their health based on criteria other
than mortality, such as disease and wellbeing.

This study cannot rule out the possibility that participants who acquired and consumed
more than the food intake analysis identified incurred greater food expenditures.
There is the additional question as to whether living longer through eating a more
diverse diet costs more. Published findings demonstrate that, for the most part, a
food-diverse diet costs more than a less diverse diet [19]. In this case, it costs more to live longer if longevity is dependent on “buying
food diversity.” This then begs the question of affordability as reported by Golan
et al. [25]. The effect of greater expenditure on vegetables and fruits to reduce mortality may
be mediated by increasing dietary diversity. Thus, both food expenditures and dietary
quality should be considered in calculating mortality risk. From food and economic
policy perspectives, providing people with nutritious and affordable food requires
further consideration.

In this study, if older adults increased food expenditure by NT$15 (or US$0.50) per
day, with vegetables they would have 12% lower all-cause mortality, and with fruit,
a 10% lower all-cause mortality. These values are even higher after the exclusion
of those who died in the first year of follow-up. A NT$15 increase for each of these
food expenditures should not to be an economic barrier for most older Taiwanese, but
may well be for the socioeconomically marginalized. The lack of this increased spending
on vegetables and fruits may represent a reluctance, rather than an inability, to
expend these amounts. This could be because of food preferences or chewing difficulty,
the latter of which appears to be the case in this cohort [15]. This study also adjusts for BMI and diabetes, which reflect energy and metabolic
disorders likely to change eating habits, whether they contribute to or are caused
by these conditions. However, these situations do not alter the place of vegetable
and fruit expenditures in mortality risk.

Households in developing countries, which spend a greater proportion of food expenditure
on grain food, tend to have more underweight children and higher under-5-year old
child mortality [12,24]. Although this study of older adults in Taiwan shows no adverse effects of grain
expenditure on mortality, there was no advantage either. This may be a reflection
of the dominant use of polished rice, rather than whole grains, in an age-group where
whole grains are likely to confer a health advantage [26]. Other factors also make the expenditure of grain in an older Asian’s diet a special
matter. As a common staple food, grain (and especially rice) has cultural significance
with its own food, health, and economic system relevance. In Taiwan, the self-sufficiency
ratio for rice is almost 100%, and its price is relatively stable [27]. The need for satiation is not usually the problem. However, an older adult’s choice
of vegetables or fruits is likely to remain a health consideration across a wide spectrum
of economic development and personal circumstances.

This study has focused on food group expenditure rather than food intake in relation
to mortality in elders. This can provide information and insight into whether food
expenditure and affordability are associated with survival. In addition, it draws
attention to the most vulnerable group.

There are some limitations to this study. First, food costs are based on a 1-d food
consumption, which might have changed over time. Since individual diets vary from
day to day, one 24-hr dietary recall might result in a less precise measurement of
usual food intake. However, for any participant, the survey day was random which might
lead to non-differential misclassification and might bias overall HR estimates toward
the null value [28-30]. Even so, we still see a significant financial effect in relation to mortality. Therefore,
with a more precise dietary method, the effect should be more evident. Moreover, Taiwanese
older adults are generally relatively stable in their dietary pattern so that the
dietary method used may not be a serious limitation [15].

The food prices in this study were derived from national average monthly prices and
did not consider regional price variations [31]. In some cases, there are retail food price differences among Taiwanese regions.
With the exception of supermarket chain prices, food prices were based on raw food
ingredients for domestic use, and did not include the cost margins for preparing food
or eating out (which is common in Taiwan). In addition, the food sources may have
been home grown or received from friends or relatives. These could result in overestimates
or underestimates of actual food costs. Because Taiwan is a relatively affluent country,
these findings may not be extrapolated to countries at different stages of economic
development or with different types of cultural food. Although the Taiwanese population
is predominantly Chinese, there are also significant indigenous populations.

Although some of the barriers to purchasing nutritious food may be overcome, as previously
shown in Taiwan [19], vegetables and fruits, which may confer a survival advantage, remain the more costly
food categories. This presents a food equity and policy dilemma. This problem may
be partly addressed by understanding how household expenditures on various foods affect
mortality rates.

Socio-demographic profiles of the population studied in relation to quintiles of vegetable
and fruit expenditure are associated with wide divergence for ethnicity (e.g., indigenous
Taiwanese) and living arrangements, although not for education or income. The ethnic
divergence is correlated with locality and region [6], with Indigenes being more mountainous and east coastal. Since plant food sources
may be more local or home-garden and less retail for Indigenes, our generalizations
may be correspondingly limited [32]. At the same time, remote communities are less likely to participate in the mainstream
food supply as studied by us. There are health risk and outcome variations across
Taiwan which may also limit our deductions [33].

In conclusion, vegetable and fruit expenditures are associated with lower mortality
among older Taiwanese adults, and may improve survival by contributing to dietary
diversity. However, there are limits to the need for these food expenditure measures
beyond the higher quintiles of intake. In the Taiwanese economy, the cost of the main
grain staple and expenditure on animal produce are not discriminant for mortality.
Although the incremental costs are currently modest, an emphasis on national nutrition
policy in Taiwan advocating affordable fruits and vegetables should improve food security
and longevity among older adults.

Competing interests

The authors declare they have no competing interests.

Authors’ contributions

All authors were involved in the study design and collectively wrote the paper; YTL
analyzed the data; MLW and MSL coordinated the research; MSL had primary responsibility
for the final content. All authors read and approved the final manuscript.

Acknowledgments

The authors are thankful for the financial support provided by the National Science
Council (NSC100-2320-B-016-005) and the National Health Research Institutes. Both
of the data sets for this study were collected for the research project “Elderly Nutrition
and Health Survey in Taiwan 1997–2002 (NAHSIT Elderly)” and National Death Registration
data sponsored by Department of Health, Executive Yuan in Taiwan. The NASHIT project
was conducted by the Institute of Biomedical Sciences of Academia Sinica and the Research
Center for Humanities and Social Sciences, Center for Survey Research, Academia Sinica,
directed by Dr. Wen-Harn Pan and Dr. Su-Hao Tu. All authors read and approved the
final manuscript.